Characteristics and Drivers of High-Altitude Ladybird Flight: Insights from Vertical-Looking Entomological Radar
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by NERC Open Research Archive Characteristics and Drivers of High-Altitude Ladybird Flight: Insights from Vertical-Looking Entomological Radar Daniel L. Jeffries1, Jason Chapman2,3, Helen E. Roy4, Stuart Humphries1, Richard Harrington2, Peter M. J. Brown5, Lori-J. Lawson Handley1* 1 Department of Biological Sciences, University of Hull, Hull, Humberside, United Kingdom, 2 Rothamsted Research, Harpenden, Hertfordshire, United Kingdom, 3 Environment and Sustainability Institute, University of Exeter, Penryn, Cornwall, United Kingdom, 4 NERC Centre for Ecology & Hydrology, Wallingford, Oxfordshire, United Kingdom, 5 Department of Life Sciences, Anglia Ruskin University, Cambridge, United Kingdom Abstract Understanding the characteristics and drivers of dispersal is crucial for predicting population dynamics, particularly in range- shifting species. Studying long-distance dispersal in insects is challenging, but recent advances in entomological radar offer unique insights. We analysed 10 years of radar data collected at Rothamsted Research, U.K., to investigate characteristics (altitude, speed, seasonal and annual trends) and drivers (aphid abundance, air temperature, wind speed and rainfall) of high-altitude flight of the two most abundant U.K. ladybird species (native Coccinella septempunctata and invasive Harmonia axyridis). These species cannot be distinguished in the radar data since their reflectivity signals overlap, and they were therefore analysed together. However, their signals do not overlap with other, abundant insects so we are confident they constitute the overwhelming majority of the analysed data. The target species were detected up to ,1100 m above ground level, where displacement speeds of up to ,60 km/h were recorded, however most ladybirds were found between ,150 and 500 m, and had a mean displacement of 30 km/h. Average flight time was estimated, using tethered flight experiments, to be 36.5 minutes, but flights of up to two hours were observed. Ladybirds are therefore potentially able to travel 18 km in a ‘‘typical’’ high-altitude flight, but up to 120 km if flying at higher altitudes, indicating a high capacity for long-distance dispersal. There were strong seasonal trends in ladybird abundance, with peaks corresponding to the highest temperatures of mid-summer, and warm air temperature was the key driver of ladybird flight. Climatic warming may therefore increase the potential for long-distance dispersal in these species. Low aphid abundance was a second significant factor, highlighting the important role of aphid population dynamics in ladybird dispersal. This research illustrates the utility of radar for studying high-altitude insect flight and has important implications for predicting long-distance dispersal. Citation: Jeffries DL, Chapman J, Roy HE, Humphries S, Harrington R, et al. (2013) Characteristics and Drivers of High-Altitude Ladybird Flight: Insights from Vertical-Looking Entomological Radar. PLoS ONE 8(12): e82278. doi:10.1371/journal.pone.0082278 Editor: Eric James Warrant, Lund University, Sweden Received June 25, 2013; Accepted October 21, 2013; Published December 18, 2013 Copyright: ß 2013 Jeffries et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was primarily funded by the Department of Biological Sciences, University of Hull. In addition, Rothamsted Research is a national instituteof bioscience strategically funded by the UK Biotechnology and Biological Sciences Research Council (BBSRC). HER is funded by the Natural Environment Research Council and also receives funding from the Joint Nature Conservation Committee. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction therefore increase the frequency and distance of migration, which, in the case of pest species, presents considerable challenges for 2 An estimated three billion insects fly through a 1 km ‘window’ conservation of native biodiversity and for sustainable agriculture. of sky in England during a typical summer month [1]. While a Ladybirds (Coleoptera: Coccinellidae) are the most abundant substantial proportion of these insects are beneficial and provide aphid predators in cereal crops worldwide, and are important essential ecosystem services, others are pests that pose a potential biological control agents of aphids and coccids [9]. However, use threat to biodiversity, the economy and human health. Knowledge of certain species in biological control has contributed to their of the characteristics (e.g. altitude and displacement speed, status as IAS in many parts of the world (see [6] and [10] for seasonal and annual trends) and drivers (e.g. prey abundance, recent reviews). For example, Coccinella septempunctata was intro- environmental factors) of insect flight is crucial for estimating long- duced to North America for biological control in the 1970s and distance dispersal capability, predicting the dynamics, persistence rapidly spread across the continent, gaining IAS status in the and spread of insect populations, and has important applications 1990s (reviewed in [1,10]). Soon afterwards (1988), another in pest management and conservation [2–6]. This knowledge is coccinellid, Harmonia axyridis, was found to be established and particularly important in the case of invasive alien species (IAS) quickly spreading in North America [6]. Since 1988, H. axyridis has and those undergoing range shifts in response to global warming established in at least 38 countries on four continents, with spread [1–7], since higher temperatures have been shown to drive rates estimated up to 500 km/year [6]. This rapid spread suggests increased migration in certain insects [8]. Global warming could considerable long-distance dispersal capability of this species, but PLOS ONE | www.plosone.org 1 December 2013 | Volume 8 | Issue 12 | e82278 Characteristics and Drivers of Ladybird Flight estimates are confounded by accidental transport by humans [6]. Both H. axyridis and C. septempunctata are considered to be strong, Studying the dispersal capability of H. axyridis is particularly active fliers with high dispersal ability, at least over short distances important given that this species has been linked to declines in [16,18,19], but studying dispersal over longer distances has been indigenous ladybirds and is thought to present a threat to native hampered by the difficulty of tracking the insects in the field. biodiversity [11,12]. Conclusions have therefore been limited to assumptions inferred Knowledge of the key characteristics of ladybird dispersal; from ground level observations of walking [21,30,31] or short- specifically flight altitude, displacement speed, and seasonal and distance flights [21,24,27,32–34], or indirect evidence for long- annual patterns, is crucial to understanding and predicting long- distance flights (e.g. from malaise-traps, [35] or mark-release- distance dispersal. Since wind speed increases with altitude, species recapture experiments, [21,36]). To our knowledge, only one that use high-altitude wind currents have greater long-distance study has so far attempted to directly study coccinellids migrating dispersal potential than those that fly only a few metres above at high altitudes. Using traps on aircraft, Hagen [37] sampled ground level (AGL), where wind currents are negligible [13]. Hippodamia convergens flying to and from migration sites, between Flight altitude is therefore a key determinant of dispersal potential. approximately 1000 and 1650 metres above ground level. Our understanding of insect seasonal phenology tends to be drawn However only 24 beetles were sampled in 15 aerial surveys. In from ground-level observations, but it is unclear whether this recent years, a new generation of vertical-looking entomological accurately reflects insect density and population dynamics. For radars (VLR) have made it possible to identify and record large instance, the number of individual records of H. axyridis from field insects flying at altitudes ,150–1200 m AGL, providing quanti- observations across the UK peaks in October, corresponding to tative estimates of insect aerial density, diversity and biomass, and the period when individuals are migrating to overwintering sites unique insights into insect population dynamics and the charac- [14], but whether this corresponds to a peak in actual abundance teristics and drivers of high-altitude [38–42] flight. Here, we is unclear. An important question is whether the potential for long- analyse VLR data collected at Rothamsted Research, Harpenden, distance dispersal is greater during the migration to or from U.K. between May-October 2000–2010, together with meteoro- overwintering sites or during the summer months, when meteo- logical and aphid suction trap data, and perform simple rological conditions may be more favourable for flight. experiments to investigate high-altitude flight in C. septempunctata Another key question is whether dispersal is driven mainly by and H. axyridis. Specifically, we investigate 1) flight characteristics biotic or environmental cues, or by a combination